Skip to main content
The Plant Cell logoLink to The Plant Cell
. 1999 Mar;11(3):393–406. doi: 10.1105/tpc.11.3.393

The CLAVATA1 receptor-like kinase requires CLAVATA3 for its assembly into a signaling complex that includes KAPP and a Rho-related protein.

A E Trotochaud 1, T Hao 1, G Wu 1, Z Yang 1, S E Clark 1
PMCID: PMC144183  PMID: 10072399

Abstract

The CLAVATA1 (CLV1) and CLAVATA3 (CLV3) genes are required to maintain the balance between cell proliferation and organ formation at the Arabidopsis shoot and flower meristems. CLV1 encodes a receptor-like protein kinase. We have found that CLV1 is present in two protein complexes in vivo. One is approximately 185 kD, and the other is approximately 450 kD. In each complex, CLV1 is part of a disulfide-linked multimer of approximately 185 kD. The 450-kD complex contains the protein phosphatase KAPP, which is a negative regulator of CLV1 signaling, and a Rho GTPase-related protein. In clv1 and clv3 mutants, CLV1 is found primarily in the 185-kD complex. We propose that CLV1 is present as an inactive disulfide-linked heterodimer and that CLV3 functions to promote the assembly of the active 450-kD complex, which then relays signal transduction through a Rho GTPase.

Full Text

The Full Text of this article is available as a PDF (683.6 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Becraft P. W., Stinard P. S., McCarty D. R. CRINKLY4: A TNFR-like receptor kinase involved in maize epidermal differentiation. Science. 1996 Sep 6;273(5280):1406–1409. doi: 10.1126/science.273.5280.1406. [DOI] [PubMed] [Google Scholar]
  2. Braun D. M., Stone J. M., Walker J. C. Interaction of the maize and Arabidopsis kinase interaction domains with a subset of receptor-like protein kinases: implications for transmembrane signaling in plants. Plant J. 1997 Jul;12(1):83–95. doi: 10.1046/j.1365-313x.1997.12010083.x. [DOI] [PubMed] [Google Scholar]
  3. Cheatham B., Kahn C. R. Insulin action and the insulin signaling network. Endocr Rev. 1995 Apr;16(2):117–142. doi: 10.1210/edrv-16-2-117. [DOI] [PubMed] [Google Scholar]
  4. Chen R. H., Derynck R. Homomeric interactions between type II transforming growth factor-beta receptors. J Biol Chem. 1994 Sep 9;269(36):22868–22874. [PubMed] [Google Scholar]
  5. Clark S. E. Organ Formation at the Vegetative Shoot Meristem. Plant Cell. 1997 Jul;9(7):1067–1076. doi: 10.1105/tpc.9.7.1067. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Clark S. E., Running M. P., Meyerowitz E. M. CLAVATA1, a regulator of meristem and flower development in Arabidopsis. Development. 1993 Oct;119(2):397–418. doi: 10.1242/dev.119.2.397. [DOI] [PubMed] [Google Scholar]
  7. Clark S. E., Williams R. W., Meyerowitz E. M. The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell. 1997 May 16;89(4):575–585. doi: 10.1016/s0092-8674(00)80239-1. [DOI] [PubMed] [Google Scholar]
  8. Dixon M. S., Jones D. A., Keddie J. S., Thomas C. M., Harrison K., Jones J. D. The tomato Cf-2 disease resistance locus comprises two functional genes encoding leucine-rich repeat proteins. Cell. 1996 Feb 9;84(3):451–459. doi: 10.1016/s0092-8674(00)81290-8. [DOI] [PubMed] [Google Scholar]
  9. Doughty J., Dixon S., Hiscock S. J., Willis A. C., Parkin I. A., Dickinson H. G. PCP-A1, a defensin-like Brassica pollen coat protein that binds the S locus glycoprotein, is the product of gametophytic gene expression. Plant Cell. 1998 Aug;10(8):1333–1347. doi: 10.1105/tpc.10.8.1333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Henis Y. I., Moustakas A., Lin H. Y., Lodish H. F. The types II and III transforming growth factor-beta receptors form homo-oligomers. J Cell Biol. 1994 Jul;126(1):139–154. doi: 10.1083/jcb.126.1.139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Horn M. A., Walker J. C. Biochemical properties of the autophosphorylation of RLK5, a receptor-like protein kinase from Arabidopsis thaliana. Biochim Biophys Acta. 1994 Sep 21;1208(1):65–74. doi: 10.1016/0167-4838(94)90160-0. [DOI] [PubMed] [Google Scholar]
  12. Jones D. A., Thomas C. M., Hammond-Kosack K. E., Balint-Kurti P. J., Jones J. D. Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science. 1994 Nov 4;266(5186):789–793. doi: 10.1126/science.7973631. [DOI] [PubMed] [Google Scholar]
  13. Kayes J. M., Clark S. E. CLAVATA2, a regulator of meristem and organ development in Arabidopsis. Development. 1998 Oct;125(19):3843–3851. doi: 10.1242/dev.125.19.3843. [DOI] [PubMed] [Google Scholar]
  14. Kieber J. J., Rothenberg M., Roman G., Feldmann K. A., Ecker J. R. CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases. Cell. 1993 Feb 12;72(3):427–441. doi: 10.1016/0092-8674(93)90119-b. [DOI] [PubMed] [Google Scholar]
  15. Laufs P., Grandjean O., Jonak C., Kiêu K., Traas J. Cellular parameters of the shoot apical meristem in Arabidopsis. Plant Cell. 1998 Aug;10(8):1375–1390. doi: 10.1105/tpc.10.8.1375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Laux T., Mayer K. F., Berger J., Jürgens G. The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development. 1996 Jan;122(1):87–96. doi: 10.1242/dev.122.1.87. [DOI] [PubMed] [Google Scholar]
  17. Li H., Wu G., Ware D., Davis K. R., Yang Z. Arabidopsis Rho-related GTPases: differential gene expression in pollen and polar localization in fission yeast. Plant Physiol. 1998 Oct;118(2):407–417. doi: 10.1104/pp.118.2.407. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Li J., Chory J. A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell. 1997 Sep 5;90(5):929–938. doi: 10.1016/s0092-8674(00)80357-8. [DOI] [PubMed] [Google Scholar]
  19. Lim L., Manser E., Leung T., Hall C. Regulation of phosphorylation pathways by p21 GTPases. The p21 Ras-related Rho subfamily and its role in phosphorylation signalling pathways. Eur J Biochem. 1996 Dec 1;242(2):171–185. doi: 10.1111/j.1432-1033.1996.0171r.x. [DOI] [PubMed] [Google Scholar]
  20. Lin Y., Wang Y., Zhu J. K., Yang Z. Localization of a Rho GTPase Implies a Role in Tip Growth and Movement of the Generative Cell in Pollen Tubes. Plant Cell. 1996 Feb;8(2):293–303. doi: 10.1105/tpc.8.2.293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lin Y., Yang Z. Inhibition of Pollen Tube Elongation by Microinjected Anti-Rop1Ps Antibodies Suggests a Crucial Role for Rho-Type GTPases in the Control of Tip Growth. Plant Cell. 1997 Sep;9(9):1647–1659. doi: 10.1105/tpc.9.9.1647. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Mayer K. F., Schoof H., Haecker A., Lenhard M., Jürgens G., Laux T. Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell. 1998 Dec 11;95(6):805–815. doi: 10.1016/s0092-8674(00)81703-1. [DOI] [PubMed] [Google Scholar]
  23. Mu J. H., Lee H. S., Kao T. H. Characterization of a pollen-expressed receptor-like kinase gene of Petunia inflata and the activity of its encoded kinase. Plant Cell. 1994 May;6(5):709–721. doi: 10.1105/tpc.6.5.709. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Schaller G. E., Ladd A. N., Lanahan M. B., Spanbauer J. M., Bleecker A. B. The ethylene response mediator ETR1 from Arabidopsis forms a disulfide-linked dimer. J Biol Chem. 1995 May 26;270(21):12526–12530. doi: 10.1074/jbc.270.21.12526. [DOI] [PubMed] [Google Scholar]
  25. Simon M. A., Dodson G. S., Rubin G. M. An SH3-SH2-SH3 protein is required for p21Ras1 activation and binds to sevenless and Sos proteins in vitro. Cell. 1993 Apr 9;73(1):169–177. doi: 10.1016/0092-8674(93)90169-q. [DOI] [PubMed] [Google Scholar]
  26. Smyth D. R., Bowman J. L., Meyerowitz E. M. Early flower development in Arabidopsis. Plant Cell. 1990 Aug;2(8):755–767. doi: 10.1105/tpc.2.8.755. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Song W. Y., Wang G. L., Chen L. L., Kim H. S., Pi L. Y., Holsten T., Gardner J., Wang B., Zhai W. X., Zhu L. H. A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science. 1995 Dec 15;270(5243):1804–1806. doi: 10.1126/science.270.5243.1804. [DOI] [PubMed] [Google Scholar]
  28. Stone J. M., Collinge M. A., Smith R. D., Horn M. A., Walker J. C. Interaction of a protein phosphatase with an Arabidopsis serine-threonine receptor kinase. Science. 1994 Nov 4;266(5186):793–795. doi: 10.1126/science.7973632. [DOI] [PubMed] [Google Scholar]
  29. Stone JM, Trotochaud AE, Walker JC, Clark SE. Control of meristem development by CLAVATA1 receptor kinase and kinase-associated protein phosphatase interactions . Plant Physiol. 1998 Aug;117(4):1217–1225. doi: 10.1104/pp.117.4.1217. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Torii K. U., Mitsukawa N., Oosumi T., Matsuura Y., Yokoyama R., Whittier R. F., Komeda Y. The Arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine-rich repeats. Plant Cell. 1996 Apr;8(4):735–746. doi: 10.1105/tpc.8.4.735. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Williams R. W., Wilson J. M., Meyerowitz E. M. A possible role for kinase-associated protein phosphatase in the Arabidopsis CLAVATA1 signaling pathway. Proc Natl Acad Sci U S A. 1997 Sep 16;94(19):10467–10472. doi: 10.1073/pnas.94.19.10467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Winge P., Brembu T., Bones A. M. Cloning and characterization of rac-like cDNAs from Arabidopsis thaliana. Plant Mol Biol. 1997 Nov;35(4):483–495. doi: 10.1023/a:1005804508902. [DOI] [PubMed] [Google Scholar]

Articles from The Plant Cell are provided here courtesy of Oxford University Press

RESOURCES